Gastrointestinal Parasite of Long-Tailed Macaque (Macaca fascicularis) in Three Different Types of Habitat

Abstract

Gastrointestinal parasite infection represents an ecological and health challenge in non-human primates. While host-parasite coevolution often maintains infections asymptomatic within natural gut communities, environmental stress and anthropogenic change can increase infection burden and disease expression. Macaca fascicularis (long-tailed macaque; LTM) exhibits high ecological plasticity across various habitat gradients, suggesting that variation in environmental conditions and human intervention may shape parasite exposure and transmission pathways. This study aims to investigate how habitat type and management practices shape gastrointestinal parasite structures by evaluating variations in prevalence, taxonomic composition, infection intensity, parasite richness, and co-infection patterns among the LTM population across natural and semi-natural habitats and a fully captive environment. Fecal sampling was conducted from November to December 2025 during the rainy season across three selected sites representing a gradient of human intervention: IPB Campus Forest Park (IPB-CFP; natural habitat), Tinjil Island (TI-PRC; semi-natural habitat), and Dramaga Captive Breeding Facility (DCBF-PRC; captive habitat). A total of 33 fresh fecal samples (11 from each site) were collected and preserved in 10% formalin. Parasitological examinations were conducted in the Pathology Laboratory of the Primate Research Center, IPB University (PRC-IPB), using both qualitative (Formalin-ethyl acetate sedimentation) and quantitative (Kato-Katz) methods. Statistical analyses, including Fisher’s exact test, Kruskal-Wallis, and Dunn’s post hoc test, were performed to assess differences in prevalence and parasite richness among three habitats. A total of eight parasite taxa were identified, comprising two protozoan (Balantioides coli and Entamoeba sp.) and six helminths (Ascaris sp., Ancylostomatidae, Oesophagostomum sp., Strongyloides sp., Trichuris sp., and Hymenolepis sp.). The overall gastrointestinal parasite prevalence was 100% at both free-ranging habitats (IPB-CFP and TI-PRC), whereas the captive population at DCBF-PRC had a lower prevalence (81.82%), with no significant difference among the three sites (p = 0.3125). However, the parasite composition differed markedly between habitats. Protozoa were detected across all sites (p = 0.3125), whereas helminths were entirely absent in DCBF-PRC (p < 0.0001). Quantitative analysis indicated light helminth infection intensities at both free-ranging sites, though parasite richness declined sharply in captivity (p < 0.001). Free-ranging habitats were dominated by multi-taxa co-infections, whereas single protozoan infections predominated in captivity. The findings indicate that the parasite community varies along the management gradient. Intensive management practice in captivity likely disrupts helminth transmission pathways. However, these protocols are less effective against the fecal-oral transmission of protozoan cysts. Conversely, both free-ranging sites have universal protozoan and helminth infections, but differed in helminth composition, likely due to microhabitat and transmission. Low infection intensity and asymptomatic carriage are consistent with subclinical coexistence between host and parasite. This study offers baseline information relevant to wildlife managers and breeding facilities that may support future management planning.

Infeksi parasit gastrointestinal merupakan tantangan ekologis dan kesehatan bagi primata non-manusia. Meskipun koevolusi antara inang dan parasit sering kali menjaga infeksi tetap asimtomatik dalam komunitas usus alami, tekanan lingkungan dan perubahan antropogenik dapat meningkatkan beban infeksi dan ekspresi penyakit. Macaca fascicularis (Monyet ekor panjang: MEP) memiliki plastisitas ekologis yang tinggi diberbagai gradien habitat, menunjukkan bahwa variasi kondisi lingkungan dan intervensi manusia dapat memengaruhi paparan parasit serta jalur penularannya. Penelitian ini bertujuan untuk menginvestigasi pengaruh tipe habitat dan praktik pengelolaan membentuk struktur parasit gastrointestinal dengan mengevaluasi variasi prevalensi, komposisi taksonomi, intensitas infeksi, kekayaan spesies, dan pola koinfeksi parasit gastrointestinal pada populasi MEP di habitat alami, semi-alami, dan lingkungan penangkaran. Pengambilan sampel dilakukan pada bulan November hingga Desember 2025, selama musim hujan, di tiga lokasi yang mewakili gradien intervensi manusia: Taman Hutan Kampus IPB (IPB-CFP; habitat alami), Stasiun Lapang Pulau Tinjil (TI-PRC; habitat semi-alami), dan Fasilitas Penangkaran Dramaga (DCBF-PRC; habitat penangkaran). Sebanyak 33 sampel feses segar (11 dari setiap lokasi) dikumpulkan ke dalam tabung yang berisi formalin 10%. Pemeriksaan parasitologi dilakukan di Laboratorium Parasitologi Pusat Studi Satwa Primata, IPB University, menggunakan metode kualitatif (sedimentasi formalin-etil asetat) dan kuantitatif (Kato-Katz). Analisis statistik (uji Fisher’s exact, Kruskal-Wallis, dan uji lanjut Dunn) dilakukan untuk menilai perbedaan prevalensi dan kekayaan parasit antara ketiga habitat. Sebanyak delapan taksa berhasil diidentifikasi, terdiri atas dua jenis protozoa (Balantioides coli dan Entamoeba sp.) serta enam jenis cacing parasit (Ascaris sp., Ancylostomatidae, Oesophagostomum sp., Strongyloides sp., Trichuris sp., dan Hymenolepis sp.). Prevalensi parasit gastrointestinal secara keseluruhan mencapai 100% pada kedua populasi liar (IPB-CFP dan TI-PRC), sedangkan populasi penangkaran di DCBF-IPB memiliki prevalensi yang lebih rendah (81,82%), tanpa perbedaan signifikan antara ketiga habitat tersebut (p = 0,3125). Namun, komposisi parasit berbeda antarhabitat. Protozoa ditemukan di semua lokasi (p = 0,3125), sedangkan cacing parasit sepenuhnya absen di DCBF-PRC (p < 0,0001). Analisis kuantitatif menunjukkan intensitas infeksi cacing parasit dalam kategori ringan pada kedua populasi liar serta penurunan signifikan kekayaan spesies parasit pada penangkaran (p < 0,001). Habitat alami dan semi-alami didominasi oleh ko-infeksi lebih dari dua taksa parasit, sementara infeksi protozoa tunggal mendominasi di penangkaran. Temuan ini menunjukkan bahwa komunitas parasit bervariansi di sepanjang gradien habitat. Praktik manajemen intensif di penangkaran berpotensi memutus jalur penularan cacing parasit. Namun, protokol tersebut belum efektif dalam mencegah penularan kista protozoa yang terjadi secara langsung melalui ingesti makanan yang terkontaminasi kista dari feses. Sebaliknya, kedua lokasi memiliki infeksi protozoa dan cacing parasit yang menyeluruh, tetapi berbeda dalam komposisi cacing parasitnya, kemungkinan disebabkan oleh mikroklimat habitat dan potensi penularannya. Infeksi tanpa gejala dan intensitas infeksi yang rendah sejalan dengan koeksistensi subklinis antara inang dan parasit. Informasi awal ini dapat membantu pengelola satwa liar dan fasilitas penangkaran dalam merencanakan pengelolaan di masa mendatang.